Determinants and Consequences of Dispersal in Vertebrates with Complex Life Cycles: a Review of Pond-Breeding Amphibians
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Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2020 Determinants and Consequences of Dispersal in Vertebrates with Complex Life Cycles: A Review of Pond-Breeding Amphibians Cayuela, Hugo ; Valenzuela-Sánchez, Andrés ; Teulier, Loïc ; Martínez-Solano, Íñigo ; Léna, Jean-Paul ; Merilä, Juha ; Muths, Erin ; Shine, Richard ; Quay, Ludivine ; Denoël, Mathieu ; Clobert, Jean ; Schmidt, Benedikt R Abstract: Dispersal is a central process in ecology and evolution. It strongly influences the dynamics of spatially structured populations and affects evolutionary processes by shaping patterns of gene flow. For these reasons, dispersal has received considerable attention from ecologists, evolutionary biologists, and conservationists. Although it has been studied extensively in taxa such as birds and mammals, much less is known about dispersal in vertebrates with complex life cycles such as pond-breeding amphibians. Over the past two decades, researchers have taken an ever-increasing interest in amphibian dispersal and initi- ated both basic and applied studies, using a broad range of experimental and observational approaches. This body of research reveals complex dispersal patterns, causations, and syndromes, with dramatic consequences for the demography and genetics of amphibian populations. In this review, our goals are to: redefine and clarify the concept of amphibian dispersal; review current knowledge about theeffects of individual (i.e., condition-dependent dispersal) and environmental (i.e., context-dependent dispersal) factors during the three stages of dispersal (i.e., emigration, transience, and immigration); identify the demographic and genetic consequences of dispersal in spatially structured amphibian populations; and propose new research avenues to extend our understanding of amphibian dispersal. DOI: https://doi.org/10.1086/707862 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-185243 Journal Article Published Version Originally published at: Cayuela, Hugo; Valenzuela-Sánchez, Andrés; Teulier, Loïc; Martínez-Solano, Íñigo; Léna, Jean-Paul; Merilä, Juha; Muths, Erin; Shine, Richard; Quay, Ludivine; Denoël, Mathieu; Clobert, Jean; Schmidt, Benedikt R (2020). Determinants and Consequences of Dispersal in Vertebrates with Complex Life Cycles: A Review of Pond-Breeding Amphibians. The Quarterly review of biology, 95(1):1-36. DOI: https://doi.org/10.1086/707862 Volume 95, No. 1 March 2020 THE QUARTERLY REVIEW of Biology DETERMINANTS AND CONSEQUENCES OF DISPERSAL IN VERTEBRATES WITH COMPLEX LIFE CYCLES: A REVIEW OF POND-BREEDING AMPHIBIANS Hugo Cayuela IBIS and Department of Biology, University Laval Quebec City, Quebec G1V 0A6 Canada e-mail: [email protected] Andrés Valenzuela-Sánchez Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile 5090000 Valdivia, Chile ONG Ranita de Darwin 8370251 Santiago, Chile Centro de Investigación para la Sustentabilidad, Facultad de Ciencias de la Vida, Universidad Andres Bello 8370251 Santiago, Chile e-mail: [email protected] Loïc Teulier UMR 5023 LEHNA, Laboratoire d’Ecologie des Hydrosystèmes Naturels et Anthropisés 69100 Villeurbanne, France e-mail: [email protected] Íñigo Martínez-Solano Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales 28006 Madrid, Spain e-mail: [email protected] The Quarterly Review of Biology, March 2020, Vol. 95, No. 1 Copyright © 2020 by The University of Chicago Press. All rights reserved. 0033-5770/2020/9501-0001$15.00 1 This content downloaded from 054.077.085.227 on February 15, 2020 01:43:39 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 2 THE QUARTERLY REVIEW OF BIOLOGY Volume 95 Jean-Paul Léna UMR 5023 LEHNA, Laboratoire d’Ecologie des Hydrosystèmes Naturels et Anthropisés 69100 Villeurbanne, France e-mail: [email protected] Juha Merilä Ecological Genetics Research Unit, Research Programme in Organismal and Evolutionary Biology, Faculty of Biological and Environmental Sciences, Department of Biosciences, University of Helsinki 00014 Helsinki, Finland e-mail: juha.merila@helsinki.fi Erin Muths Fort Collins Science Center, U.S. Geological Survey Fort Collins, Colorado 80526 USA e-mail: [email protected] Richard Shine School of Life and Environmental Sciences, University of Sydney Sydney, New South Wales 2006 Australia e-mail: [email protected] Ludivine Quay Nature, Ecology and Conservation 73000 Montagnole, France e-mail: [email protected] Mathieu Denoël Laboratory of Ecology and Conservation of Amphibians (LECA), Freshwater and Oceanic Science Unit of Research (FOCUS), University of Liège 4000 Liège, Belgium e-mail: [email protected] Jean Clobert Theoretical and Experimental Ecology Station (UMR 5371), National Centre for Scientific Research (CNRS), Paul Sabatier University (UPS) 09200 Moulis, France e-mail: [email protected] This content downloaded from 054.077.085.227 on February 15, 2020 01:43:39 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). March 2020 DISPERSAL OF AMPHIBIANS 3 Benedikt R. Schmidt Institut für Evolutionsbiologie und Umweltwissenschaften, Universität Zürich 8057 Zürich, Switzerland Info fauna karch 2000 Neuchâtel, Switzerland e-mail: [email protected] keywords dispersal syndromes, demography, landscape genetics, movement, emigration, immigration, transience abstract Dispersal is a central process in ecology and evolution. It strongly influences the dynamics of spa- tially structured populations and affects evolutionary processes by shaping patterns of gene flow. For these reasons, dispersal has received considerable attention from ecologists, evolutionary biologists, and conservationists. Although it has been studied extensively in taxa such as birds and mammals, much less is known about dispersal in vertebrates with complex life cycles such as pond-breeding amphib- ians. Over the past two decades, researchers have taken an ever-increasing interest in amphibian dis- persal and initiated both basic and applied studies, using a broad range of experimental and observational approaches. This body of research reveals complex dispersal patterns, causations, and syn- dromes, with dramatic consequences for the demography and genetics of amphibian populations. In this review, our goals are to: redefine and clarify the concept of amphibian dispersal; review current knowl- edge about the effects of individual (i.e., condition-dependent dispersal) and environmental (i.e., con- text-dependent dispersal) factors during the three stages of dispersal (i.e., emigration, transience, and immigration); identify the demographic and genetic consequences of dispersal in spatially structured amphibian populations; and propose new research avenues to extend our understanding of amphibian dispersal. Introduction zation-extinction dynamics in heterogenous ISPERSAL describes the unidirec- landscapes (Hanski and Gilpin 1991; Gilpin D tional movement of an individual from 2012). Dispersal also has relevance beyond its natal site to its breeding site (i.e., natal dis- ecology. Successful reproduction following persal) and between breeding sites (i.e., dispersal results in gene flow between popu- breeding dispersal; Clobert et al. 2009; lations (Ronce 2007; Broquet and Petit 2009; Matthysen 2012). Dispersal is a central mech- Lowe and Allenford 2010) that can strongly anism in ecology and evolution that has re- influence adaptive processes (Ronce 2007; ceived considerable attention (Gadgil 1971; Legrand et al. 2017). Through gene flow, dis- fi Johnson and Gaines 1990; Clobert et al. 2001, persal modi es effective population size (Ne) 2012a; Ronce 2007). It is recognized as being and regulates the effects of genetic drift critical to the dynamics of spatially structured and the effectiveness of selection, influencing populations (Hanski and Gilpin 1991; Thomas the likelihood and pace of local adaptation and Kunin 1999; Clobert et al. 2009). Dis- (Ronce 2007; Broquet and Petit 2009) and persal affects demographic interdependence even speciation (Marques et al. 2019). among populations and local population Dispersal can be considered as a three- growth (Thomas and Kunin 1999; Lowe and stage process: emigration (departure), tran- Allendorf 2010; Gilpin 2012). It is also impor- sience (movement in the landscape matrix), tant for the colonization of empty patches and immigration (arrival; Baguette and Van and, therefore, plays a central role in coloni- Dyck 2007; Clobert et al. 2009; Matthysen This content downloaded from 054.077.085.227 on February 15, 2020 01:43:39 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 4 THE QUARTERLY REVIEW OF BIOLOGY Volume 95 2012). The evolution of dispersal is shaped sis; Wilbur 1980) and an ontogenetic niche by the balance between the relative costs shift (Werner and Gilliam 1984). In such or- and benefits associated with leaving (dispers- ganisms, conditions during early ontogenetic ing) versus staying (not dispersing; Stamps stages can dramatically influence the dispersal et al. 2005; Bonte et al. 2012). This cost-ben- process taking place after metamorphosis; in- efit balance can be influenced by individual deed, environmental conditions (e.g., water